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Determinants of functional coupling between astrocytes and respiratory neurons in the pre-Bötzinger complex.

Schnell C, Fresemann J, Hülsmann S - PLoS ONE (2011)

Bottom Line: In astrocytes that exhibited rhythmic potassium fluxes and glutamate transporter currents, we did not find a translation of respiratory neuronal activity into phase-locked astroglial calcium signals.We conclude that astrocytes do not exhibit respiratory-rhythmic calcium fluctuations when they are able to prevent synaptic glutamate accumulation.Calcium signaling is, however, observed when glutamate transport processes in astrocytes are suppressed or neuronal discharge activity is excessive.

View Article: PubMed Central - PubMed

Affiliation: Abt. Neuro- und Sinnesphysiologie, Zentrum Physiologie und Pathophysiologie, Georg-August-Universität, Göttingen, Germany.

ABSTRACT
Respiratory neuronal network activity is thought to require efficient functioning of astrocytes. Here, we analyzed neuron-astrocyte communication in the pre-Bötzinger Complex (preBötC) of rhythmic slice preparations from neonatal mice. In astrocytes that exhibited rhythmic potassium fluxes and glutamate transporter currents, we did not find a translation of respiratory neuronal activity into phase-locked astroglial calcium signals. In up to 20% of astrocytes, 2-photon calcium imaging revealed spontaneous calcium fluctuations, although with no correlation to neuronal activity. Calcium signals could be elicited in preBötC astrocytes by metabotropic glutamate receptor activation or after inhibition of glial glutamate uptake. In the latter case, astrocyte calcium elevation preceded a surge of respiratory neuron discharge activity followed by network failure. We conclude that astrocytes do not exhibit respiratory-rhythmic calcium fluctuations when they are able to prevent synaptic glutamate accumulation. Calcium signaling is, however, observed when glutamate transport processes in astrocytes are suppressed or neuronal discharge activity is excessive.

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Astrocytes do not exhibit rhythmic calcium signals.(A) Current steps evoked in a EGFP-expressing astrocyte by depolarizing and hyperpolarizing voltage steps (10 mV increments) from a holding potential of −70 mV to potentials between −150 to +30 mV. This type of current responses to voltage steps is typical for a passive astrocyte. Panel (B) shows calcium signals (ΔF/F0) and membrane current (pA) recorded from the particular astrocyte characterized in panel (A), along with simultaneously recorded field potentials (preBötC ∫). In this example, the fluorometric calcium signals (B, Cc) were obtained with Calcium orange (200 µM) loaded via the recording pipette. Rhythmic current fluctuations are buried in the noise but are unmasked by cycle triggered averaging in (C). No phase-locked astrocytic calcium signal could be detected.
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pone-0026309-g004: Astrocytes do not exhibit rhythmic calcium signals.(A) Current steps evoked in a EGFP-expressing astrocyte by depolarizing and hyperpolarizing voltage steps (10 mV increments) from a holding potential of −70 mV to potentials between −150 to +30 mV. This type of current responses to voltage steps is typical for a passive astrocyte. Panel (B) shows calcium signals (ΔF/F0) and membrane current (pA) recorded from the particular astrocyte characterized in panel (A), along with simultaneously recorded field potentials (preBötC ∫). In this example, the fluorometric calcium signals (B, Cc) were obtained with Calcium orange (200 µM) loaded via the recording pipette. Rhythmic current fluctuations are buried in the noise but are unmasked by cycle triggered averaging in (C). No phase-locked astrocytic calcium signal could be detected.

Mentions: We recorded from 15 voltage-clamped astrocytes that exhibited rhythmic inward current fluctuations and were dialyzed with calcium indicator dye through the patch pipette. Cycle averaged Iresp,A amplitude was −3.17±3.88 pA. Calcium signals synchronized with preBötC field potentials were detected neither in the soma (figure 4) nor in the dendritic compartments of the astrocytes.


Determinants of functional coupling between astrocytes and respiratory neurons in the pre-Bötzinger complex.

Schnell C, Fresemann J, Hülsmann S - PLoS ONE (2011)

Astrocytes do not exhibit rhythmic calcium signals.(A) Current steps evoked in a EGFP-expressing astrocyte by depolarizing and hyperpolarizing voltage steps (10 mV increments) from a holding potential of −70 mV to potentials between −150 to +30 mV. This type of current responses to voltage steps is typical for a passive astrocyte. Panel (B) shows calcium signals (ΔF/F0) and membrane current (pA) recorded from the particular astrocyte characterized in panel (A), along with simultaneously recorded field potentials (preBötC ∫). In this example, the fluorometric calcium signals (B, Cc) were obtained with Calcium orange (200 µM) loaded via the recording pipette. Rhythmic current fluctuations are buried in the noise but are unmasked by cycle triggered averaging in (C). No phase-locked astrocytic calcium signal could be detected.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3198395&req=5

pone-0026309-g004: Astrocytes do not exhibit rhythmic calcium signals.(A) Current steps evoked in a EGFP-expressing astrocyte by depolarizing and hyperpolarizing voltage steps (10 mV increments) from a holding potential of −70 mV to potentials between −150 to +30 mV. This type of current responses to voltage steps is typical for a passive astrocyte. Panel (B) shows calcium signals (ΔF/F0) and membrane current (pA) recorded from the particular astrocyte characterized in panel (A), along with simultaneously recorded field potentials (preBötC ∫). In this example, the fluorometric calcium signals (B, Cc) were obtained with Calcium orange (200 µM) loaded via the recording pipette. Rhythmic current fluctuations are buried in the noise but are unmasked by cycle triggered averaging in (C). No phase-locked astrocytic calcium signal could be detected.
Mentions: We recorded from 15 voltage-clamped astrocytes that exhibited rhythmic inward current fluctuations and were dialyzed with calcium indicator dye through the patch pipette. Cycle averaged Iresp,A amplitude was −3.17±3.88 pA. Calcium signals synchronized with preBötC field potentials were detected neither in the soma (figure 4) nor in the dendritic compartments of the astrocytes.

Bottom Line: In astrocytes that exhibited rhythmic potassium fluxes and glutamate transporter currents, we did not find a translation of respiratory neuronal activity into phase-locked astroglial calcium signals.We conclude that astrocytes do not exhibit respiratory-rhythmic calcium fluctuations when they are able to prevent synaptic glutamate accumulation.Calcium signaling is, however, observed when glutamate transport processes in astrocytes are suppressed or neuronal discharge activity is excessive.

View Article: PubMed Central - PubMed

Affiliation: Abt. Neuro- und Sinnesphysiologie, Zentrum Physiologie und Pathophysiologie, Georg-August-Universität, Göttingen, Germany.

ABSTRACT
Respiratory neuronal network activity is thought to require efficient functioning of astrocytes. Here, we analyzed neuron-astrocyte communication in the pre-Bötzinger Complex (preBötC) of rhythmic slice preparations from neonatal mice. In astrocytes that exhibited rhythmic potassium fluxes and glutamate transporter currents, we did not find a translation of respiratory neuronal activity into phase-locked astroglial calcium signals. In up to 20% of astrocytes, 2-photon calcium imaging revealed spontaneous calcium fluctuations, although with no correlation to neuronal activity. Calcium signals could be elicited in preBötC astrocytes by metabotropic glutamate receptor activation or after inhibition of glial glutamate uptake. In the latter case, astrocyte calcium elevation preceded a surge of respiratory neuron discharge activity followed by network failure. We conclude that astrocytes do not exhibit respiratory-rhythmic calcium fluctuations when they are able to prevent synaptic glutamate accumulation. Calcium signaling is, however, observed when glutamate transport processes in astrocytes are suppressed or neuronal discharge activity is excessive.

Show MeSH
Related in: MedlinePlus